ORIGINAL RESEARCH ARTICLEpublished: 10 June 2014

doi: 10.3389/fnbeh.2014.00209

Improvement of mood and sleep alterations inposttraumatic stress disorder patients by eye movementdesensitization and reprocessingMara R. Raboni1, Fabiana F. D. Alonso2, Sergio Tufik3 and Deborah Suchecki1*

1 Group of Studies on the Neurobiology of Stress and Stress-Related Disorders, Departamento de Psicobiologia, Universidade Federal de São Paulo, São Paulo,Brazil

2 Instituto do Sono, Associação Fundo de Incentivo à Pesquisa, São Paulo, Brazil3 Sleep Division, Departamento de Psicobiologia, Universidade Federal de São Paulo, São Paulo, Brazil

Edited by:

Francesca Cirulli, Istituto Superioredi Sanità, Italy

Reviewed by:

Thomas Fenzl, University ofInnsbruck, AustriaFiona Hollis, Ecole PolytechniqueFederale de Lausanne, Switzerland

*Correspondence:

Deborah Suchecki, Departamentode Psicobiologia, UniversidadeFederal de São Paulo, Rua Napoleãode Barros, 925, Vila Clementino –São Paulo, 04024-002, Brazile-mail: deborah.suchecki@gmail.com

Posttraumatic stress disorder (PTSD) patients exhibit depressive and anxiety symptoms,in addition to nightmares, which interfere with sleep continuity. Pharmacologic treatmentof these sleep problems improves PTSD symptoms, but very few studies have usedpsychotherapeutic interventions to treat PTSD and examined their effects on sleepquality. Therefore, in the present study, we sought to investigate the effects of EyeMovement Desensitization Reprocessing therapy on indices of mood, anxiety, subjective,and objective sleep. The sample was composed of 11 healthy controls and 13 PTSDpatients that were victims of assault and/or kidnapping. All participants were assessedbefore, and 1 day after, the end of treatment for depressive and anxiety profile, generalwell-being and subjective sleep by filling out specific questionnaires. In addition, objectivesleep patterns were evaluated by polysomnographic recording. Healthy volunteers weresubmitted to the therapy for three weekly sessions, whereas PTSD patients underwentfive sessions, on average. Before treatment, PTSD patients exhibited high levels ofanxiety and depression, poor quality of life and poor sleep, assessed both subjectivelyand objectively; the latter was reflected by increased time of waking after sleep onset.After completion of treatment, patients exhibited improvement in depression and anxietysymptoms, and in quality of life; with indices that were no longer different from controlvolunteers. Moreover, these patients showed more consolidated sleep, with reduction oftime spent awake after sleep onset. In conclusion, Eye Movement Desensitization andReprocessing was an effective treatment of PTSD patients and improved the associatedsleep and psychological symptoms.

Keywords: Posttraumatic stress disorder, EMDR, psychotherapy, depression, anxiety, sleep fragmentation

INTRODUCTIONPosttraumatic stress disorder (PTSD) is the only psychiatric disor-der in which a psychosocial stressor is the explicit etiologic factor(Olff et al., 2005). More than two thirds of the world’s popula-tion are exposed to traumatic events at least once in their life,but only a small portion develops PTSD (Kessler et al., 1995;Breslau et al., 1998; Creamer et al., 2001; Norris et al., 2001), witha fourfold higher prevalence in women than in men (Stein et al.,1997). In addition, a high prevalence of co-morbidity with panic,agoraphobia, obsessive-compulsive disorder, major depression,somatization, and drug abuse has been reported (DSM-IV, 1994).This variability depends on individual characteristics, such as per-sonality, perception of the traumatic event and coping strategies(Olff et al., 2005).

According to the DSM-IV, the chronic form of PTSD is char-acterized by the presence of symptoms, minimally after 3 monthsof the traumatic event, and the most significant ones include re-experiencing the traumatic event, with recurrent and intrusiverecollections (flashbacks) and/or distressing dreams of the event,

physiological reactivity upon exposure to internal or external cuesthat resemble the event or exposure to situational reminders,persistent avoidance of trauma-related stimuli, restricted rangeof affect, symptoms of increased arousal, including hypervigi-lance, and exaggerated startle response (DSM-IV, 1994). PTSDpatients present with reduced parasympathetic tonus, on the onehand, and augmented sympathetic activity (Cohen et al., 1997;Rothbaum et al., 2001; Blechert et al., 2007) on the other, whichmay explain, at least in part, the arousal and hypervigilancecharacteristic of this condition (Mellman et al., 1995c).

Currently, sleep alterations, particularly those involving REMsleep (Mellman et al., 2002), such as increased REM density(Mellman et al., 1995a; Pillar et al., 2000) are considered hall-marks of PTSD (Hefez et al., 1987; Ross et al., 1989; Spoormakerand Montgomery, 2008). Co-morbidity between PTSD and sleepcomplaints reaches impressive rates (Kato et al., 1996; Ohayonand Shapiro, 2000; Pillar et al., 2000), and this is particularlyrelevant for a disorder that involves stressful situations, sincesleep has been proposed to be a natural form of resetting the

Frontiers in Behavioral Neuroscience www.frontiersin.org June 2014 | Volume 8 | Article 209 | 1

BEHAVIORAL NEUROSCIENCE

Raboni et al. EMDR, sleep and PTSD patients

activity of stress response systems, whereas sleep deprivation orpoor sleep augments the activity of these systems (Suchecki et al.,2012). Moreover, recent findings point to the possibility thatsleep disorders may not only be a consequence (Spoormakerand Montgomery, 2008), but also a precipitating factor of PTSD(Bryant et al., 2010; Van Liempt, 2012). Therefore, PTSD patientsmay be under the control of a vicious circle that involves poorsleep quality leading to exacerbated stress response, which resultsin worsening of sleep.

One way of breaking this vicious circle is to treat one of theconditions and examine the outcome on the other. On the onehand, both pharmacological and psychological treatments forsleep disorders have been shown to improve PTSD symptoms(Krakow et al., 2001a,b, 2002; Germain et al., 2012). Conversely,treatment of PTSD, by different kinds of psychotherapy hasyielded controversial results. Reports indicate that althoughpatients exhibit improvement of PTSD symptoms, sleep prob-lems, such as insomnia (Zayfert and Deviva, 2004) and poorsleep quality (Galovski et al., 2009) still persist. Importantly,these studies have only assessed subjective sleep. In a recentstudy, an 8-week period of Cognitive Behavioral Therapy (CBT)for insomnia was offered to PTSD patients, producing subjec-tive and objective improvement of sleep, depressive symptomsand social adjustment (Talbot et al., 2014). To the best of ourknowledge, no study had evaluated the effects of Eye MovementDesensitization and Reprocessing (EMDR®) on subjective sleepcomplaints and objective sleep pattern in PTSD patients. Wechose to employ EMDR given the evidence that this treatment,together with trauma focused CBT, is effective in reducing clin-ician assessed PTSD symptoms (Van Etten and Taylor, 1998;Bisson and Andrew, 2007; Bisson et al., 2007; Rhudy et al., 2010).This psychotherapy involves alternated bilateral sensorial stimula-tion at the same time that the traumatic event is being processed(Shapiro, 1996). According to Francine Shapiro, who developedthe therapy, “Processing (or reprocessing) is thus defined as theforging of the associations required for learning to take placeas the information pertaining to the traumatic event is adap-tively resolved” (Shapiro, 1999), e.g., when the patient ceasesto present emotional reactions while retrieving the traumaticsituation.

The present study was, therefore, carried out to test thehypothesis that treatment of PTSD with EMDR would improvethe patients’ psychological and general well being, and sleepquality measured both objectively and subjectively.

METHODSSUBJECTSPatients (PTSD group) and healthy volunteers (Control, CTL—group) were recruited from May 10, 2004 to July 2, 2008, bynewspaper, TV and radio announcements, followed by referralfrom selected participants. All subjects were informed of thestudy objectives and procedures, as well as the possible benefitsof EMDR. Those interested in participating in the study signedan informed consent form and all procedures were approved bythe Ethics Research Committee of Universidade Federal de SãoPaulo, in accordance with the Declaration of Helsinki (CEP #354/03). Because this study commenced before the requirement

of registration in Clinical Trials, it was only registered last year(http://www.ensaiosclinicos.gov.br/rg/edit/1456/), and approvalis still pending.

Healthy control volunteers were enrolled to match the patients,as close as possible, for age, sex, and educational level. No finan-cial incentive was provided to increase adherence to the protocol.All participants were capable of understanding the objectives andprocedures involved in this study.

INCLUSION CRITERIAThe traumatic event was restricted to assault and/or kidnappingwhich took place within 3 months to 5 years prior to enrollmentin the study. Participants were of both sexes, 24–40 years old andwere, at least, high school graduates, BMI < 30 kg/m2 and livingin São Paulo City. This time frame was chosen based on DSM-IVcriteria for chronic PTSD symptoms (duration for 3 months ormore) (DSM-IV, 1994).

Participants answered questions regarding the traumatic eventand how long ago it occurred, as well as demographic data, suchas age, years of school, sex, and occupation. All participants wereinterviewed to confirm whether they fulfilled the required crite-ria to participate in the study (as described above) and eligibleones were treated by the psychologist in charge (MRR) in theclinical center of the Department of Psychobiology. All partici-pants were submitted to a psychiatric evaluation for confirmationof PTSD diagnosis and absence of any psychiatric conditions forthe CTL group. Psychiatric interview consisted of application ofthe Structured Clinical Interview for DSM-IV Axis I Disorders(SCID-I), translated and validated to Brazilian Portuguese (DelBen et al., 2001).

Initially, 24 PTSD patients were enrolled in the study; how-ever, 11 were not included in the final analyses because they:(1) reported illnesses diagnosed after the onset of treatment(hyperthyroidism); (2) were victims of more than one traumaticevent different from the specific one (sexual assault, job accident,domestic violence); (3) missed EMDR sessions due to work com-mitments; (4) experienced stressful life events, such as divorce,home or town moving and work change. Even though thesepatients were excluded from the study, they were offered to con-tinue the treatment, but only five did so. The final sample size,therefore, included twenty-four subjects, 11 healthy volunteers(CTL group) and 13 PTSD patients (PTSD group).

EXCLUSION CRITERIAThe following were used as exclusion criteria: (1) use of any med-ication that could interfere with sleep architecture; (2) use ofpsychotropic drugs; (3) use of any medication that could increaserapid eye movements; (4) clinical and neurologic disorders; (5)past history of neurologic, endocrine or hepatic disease; (6) dis-sociative disorders or psychosis; and (7) history of sleep disorder(either assessed objectively or reported by the patient) previous tothe traumatic event.

QUESTIONNAIRESVolunteers and patients filled out the questionnaires listed below,before and after the end of treatment. All questionnaires werevalidated for Brazilian Portuguese.

Frontiers in Behavioral Neuroscience www.frontiersin.org June 2014 | Volume 8 | Article 209 | 2

Raboni et al. EMDR, sleep and PTSD patients

• Questionnaire of social-economic status (ABIPEME, 2003), wasused to assess social-economic status according to the BrazilianAssociation of Market Research Institutes. This is an instru-ment that classifies the subject in social categories accord-ing to his/her economic status and level of education. Thefive social classes range from A to E, class E being thelowest.

• Impact of Event Scale (Horowitz et al., 1979): was used to mea-sure the impact of the traumatic event that contributed totriggering PTSD. It identifies intrusive and avoidance symp-toms following the traumatic event. It was also used to assessthe effects of reprocessing during each session of EMDR.

• Beck Depression Inventory (Beck et al., 1961): is a 21-itemself-reported inventory designed to measure the severity ofdepression. Scores can range from 0 to 63, and are classifiedas follows: minimal, 0–11; mild, 12–19; moderate, 20–35; andsevere, 36–63.

• State Trait Anxiety Inventory (Spielberger et al., 1970): is com-posed of two scales: state-anxiety and trait-anxiety and eachscale contains 20 items, in which the subject marks how he/sheusually feels (trait) or how he/she feels at that time (state).

• Recovery-Stress-Questionnaire – RESTQ-48 (Kellmann andKallus, 2001): was used to assess the level of stress with the pur-pose of monitoring the recovery capacity from psychologicaland physical stressors in the last 7 days. It is composed of 12general scales used to gather information about the emotional,personal, social, and work routines of the subject. Among thequestions, those related to sleep are: (19) I feel fresh, satisfiedand relaxed; (27) I slept well; (36) I had a restless sleep; (46)My sleep was easily disturbed. Subjects attributed a score from0 to 6 to each question of the questionnaire and a median wascalculated. All aspects were assessed together and a final scorewas reached.

• Pittsburgh Sleep Quality Index (Buysse et al., 1989), was used toassess the patients and volunteers subjective sleep quality andtheir sleep habits. It has seven components—subjective qualityof sleep, latency to sleep, sleep duration, sleep efficiency, sleepdisorders, use of sleeping medication and daytime sleepiness—which result in a score of global subjective sleep quality. Theglobal score is determined by the sum of all components, vary-ing from 0 to 3, where 3 is the most negative in a Likert-typescale. The score ranges from 0 to 21, those higher than fivebeing an indication of bad sleep quality.

• SF-36 Life Quality (Ware and Sherbourne, 1992): is composedof 11 questions and 36 items that encompass eight dimensionsrepresented by functional capacity, physical aspects, pain, gen-eral health status, vitality, social aspects, emotional aspects,mental health, and one comparative question about currentand past (last year) health perception. In each dimension, scorevaries from 0 (worst) to 100 (best).

• Scale of social adjustment (Weissman and Bothwell, 1976): Thisscale is composed of 54 questions, 42 of which are relatedto work and the subject must answer six out of 18 questionsregarding his/her main occupation. The items assess aspectsof performance and quality of interpersonal relationships andfeelings of personal fulfillment in the last 2 weeks. The lowerthe score, the better the social adjustment.

• Subjective Units of Distress Scale (SUD): This scale is used toassess the patient’s discomfort at the beginning and end ofeach EMDR session. The patient attributes a score from 0 to10, where 0 represents no distress and 10 represent the highestdistress possible.

OBJECTIVE SLEEP ASSESSMENTObjective sleep evaluation was carried out, individually, by whole-night polysomnography in the Sleep Institute, by technical spe-cialized personnel, on three nights: Night 1: Adaptation to thelaboratory and to recording cables and equipment; Night 2: Basalpolysomnography, before the onset of EMDR treatment (PSG1) and Night 3: Post-treatment recording, performed on thenight following the end of treatment (PSG 2). Polysomnographywas performed with three channels of electroencephalogram(EEG: C3-A2; C4-A1; O2-A1), two channels of electrooculo-gram (EOG), one submental and one tibial electromyogram,and one electrocardiogram. Sleep scoring was performed accord-ing to Rechstchaffen and Kales (Rechtschaffen and Kales, 1968),using 30 s epochs. Wakening and respiratory events and peri-odic leg movements were considered according to the guide-lines of the American Sleep Disorders Association and theAmerican Association of Sleep Medicine (AASM, 1999; ASDA,2003).

The following parameters were obtained by the polysomnog-raphy (PSG): (1) Sleep latency (min): interval between the onsetof the recording and the first epoch of stage 2; (2) Latencyto REM sleep (min): time interval between sleep onset andthe first REM episode; (3) Total sleep time (TST - min): timeinterval between sleep onset and offset, excluding all periods ofawakening; (4) Sleep efficiency (%): Percentage of TST duringtotal recording time; (5) Sleep stages (N1, N2, N3, and REM):expressed as percentage of TST; (6) REM density: visual count-ing of rapid eye movements (above 25 µV) during each period ofREM sleep; and (7) Time of waking after sleep onset (WASO, inmin): sum of all periods of waking after sleep initiation. Womenwere sleep recorded between the 6th and 25th day of the men-strual cycle. In order to examine the sequence of sleep stages,as an additional evaluation of sleep continuity, polysomnogramswere inspected individually and transitions between REM sleepand waking, REM sleep and N1, and REM sleep and N2 werecounted.

An accredited polysomnography technician, blind to the groupcondition, analyzed the sleep recordings.

EMDR PROCEDUREEMDR treatment was applied according to the protocol estab-lished by Shapiro (Shapiro, 1995) and following the guidelinesestablished by Foa and Meadows (Foa and Meadows, 1997).The individual session began with a brief explanation of thetechnique. Subjects of the PTSD group were asked to recall atrauma-related scene or image, whereas Control subjects wereasked to recall an aversive or highly unpleasant situation. Eachvolunteer was asked to identify a physical feeling or sensation,negative and positive beliefs related to the trauma. PTSD patientswere asked to assess his/her level of discomfort in a Likert-typescale from 0 to 10, the negative belief in the SUD scale and

Frontiers in Behavioral Neuroscience www.frontiersin.org June 2014 | Volume 8 | Article 209 | 3

Raboni et al. EMDR, sleep and PTSD patients

the desired positive belief of this event, in a 1-7 scale, where1 represents completely false and 7, completely true. After thisinitial evaluation the bilateral stimulation began (guided eyemovement through horizontal motion of the therapist’s arm oralternated tapping on the patient’s knees) and after approxi-mately 12 motions the patients were asked to report new scenesand reevaluate physical sensations and feelings. At the end ofthe session, the therapist (MRR) checked the patient’s condi-tion and if complete sensitization of the material (SUD < 1)had occurred. If it had not, the session was wrapped up with a“safe place” relaxation technique. It is worth mentioning that dur-ing EMDR, the traumatic memory, as well as feelings, emotions,ideas, images, and behaviors related to this memory emerge, sothe patient can face and process the trauma, under a safe situa-tion. Therefore, re-experiencing the trauma is extremely intenseto patients, regardless of how long he/she was exposed to thetrauma.

Each weekly session lasted approximately 90 min, and sub-jects attended a minimum of three to a maximum of 10 sessions,depending on their self-report improvement during the repro-cessing and resolution of the traumatic experience, which wereclassified as: negative emotions (fear, insecurity, despair, sadness,anguish, impotence, disgust, tension, stress, guilt, discomfort),positive emotions (tranquility, relaxation, relief, self-control, cau-tion, happiness, overcoming, well-being, hope, freedom, feelingsof safety, lightness) and anger. Heart rate was recorded in PTSDpatients, during each therapy session by a Polar™ monitor con-nected to a chest belt, every 10 min, together with a report of thepredominant feeling among the abovementioned ones.

Subjects in PTSD and Control groups came in for a firstvisit, when they were informed about the procedures, signed theinformed consent and filled out the psychological profile ques-tionnaires. They were scheduled for two consecutive nights ofPSG before beginning EMDR sessions. On the night after the lastEMDR session, the subjects underwent a final PSG and filled outthe questionnaires once again. The whole treatment lasted twoand a half months, on average. Figure 1 shows the flow chartdiagram of the present study.

STATISTICAL ANALYSISFor psychological variables, between group comparisons (CTL ×PTSD in each phase) were carried out by the Mann-WhitneyU test, whereas within group comparisons (before x after treat-ment), by the Wilcoxon paired test. Objective sleep parame-ters were analyzed by a Two-Way repeated ANOVA with group(CTL, PTSD) and time-point (repeated measure: before, aftertreatment) as main factors. Heart rate was analyzed by aOne-Way ANOVA for repeated measures, with time-point (ses-sions 1 through 5) as the main factor. Post-hoc analysis wasdone by the Newman-Keuls Test and the level of significanceadopted was p < 0.05; the software used was Statistica v. 7.0(Copyright© StatSoft, Inc.). Cohen’s D effect size was calcu-lated for all sleep parameters. This is an index that measuresthe magnitude of an effect and the calculator is available athttp://www.uccs.edu/∼faculty/lbecker/. Values of 0.5–0.8 repre-sent moderate relevance, whereas those above 0.81, high relevance(http://www.uccs.edu/∼faculty/lbecker/es.htm).

RESULTSThere were no differences between groups in regard to the ratio ofwomen:men, age, socio-economic status and education (Table 1).Eleven PTSD patients dropped out of the study for several rea-sons, including: illnesses revealed after the onset of treatment;patients who reported having being exposed to more than onetraumatic event; patients who missed more than one therapy ses-sion or had family problems that precluded their adherence to thetreatment.

PSYCHOLOGICAL WELL-BEING AND OBJECTIVE SLEEPTable 2 shows the results of psychological, stress perception andwell-being assessments. Regarding the impact of the event, natu-rally, PTSD patients showed higher scores than CTL group (p <

0.002) before the beginning of treatment (U = 16.5; p < 0.002).These differences were no longer detectable after the treatment,but the comparison between before and after treatment showedthat the impact of the event was reduced in all groups (p < 0.05).

Depression scores were also different between the groupsbefore the onset of treatment (U = 5.5; p < 0.0005), with higherscores for PTSD patients than CTL subjects. After treatment, thegroups were no longer different, and PTSD patients exhibitedlower levels of depression than before treatment (p < 0.002).

Before treatment, the level of state-anxiety (U = 23.5; p <

0.006) was greater in PTSD than in CTL group, but this was nolonger observed after the treatment. Regarding the level of trait-anxiety, PTSD patients showed higher scores than CTL group(U = 8.5; p < 0.0003). Again, trait-anxiety did not differ amongthe groups after the treatment, with PTSD patients exhibitingreduction of both state and trait anxiety, following treatment(p < 0.005 in both cases).

The results of perception of general stress showed differencesbetween the groups before treatment (U = 10; p < 0.0005), inwhich PTSD group had higher scores than the CTL group, butthis difference was no longer observed after EMDR. Regardingemotional stress, the results were similar to those of general stress(U = 6.0; p < 0.0002). Before treatment, a significant differencewas observed in the social stress domain (U = 16.0; p < 0.002)and fatigue (U = 34.0; p < 0.04), with PTSD group showinghigher scores than the CTL group in both domains. These dif-ferences were not observed after EMDR. In view of these results,the general well-being was different between the groups (U = 8.0;p < 0.0003), and PTSD patients exhibited the worst conditionbefore treatment.

According to the SF-36 questionnaire, prior to treatmentPTSD patients exhibited worse quality of life than the CTL group(U = 2.0; p < 0.0001). No differences among the groups wereobserved after the treatment.

The groups also differed in social adjustment, both before(U = 10.0; p < 0.0004) and after the treatment (U = 35.0; p <

0.04); PTSD patients exhibited higher scores than CTL subjects,e.g., poor social adjustment, (p < 0.0003), but after EMDR therewas an improvement in this parameter for PTSD patients (p <

0.02).Self-assessment of sleep quality in the RESTQ-48 question-

naire (Figure 2A) showed differences among the groups (U =13.0; p < 0.0008); PTSD patients evaluated their sleep as being

Frontiers in Behavioral Neuroscience www.frontiersin.org June 2014 | Volume 8 | Article 209 | 4

Raboni et al. EMDR, sleep and PTSD patients

FIGURE 1 | Flow chart indicating the total number of individuals assessed, recruited and treated by EMDR (CONSORT).

worse than the CTL (p < 0.001) group. After the treatment, thepatients attributed an improvement to their sleep (p < 0.002).

A similar result was obtained with the Pittsburg Sleep IndexQuality (Figure 2B) (U = 17.0; p < 0.002); before treatment

PTSD patients self-rated their sleep quality as being worsethan that of CTL subjects (p < 0.003). After the treatment,PTSD patients did not exhibit any difference from healthyvolunteers.

Frontiers in Behavioral Neuroscience www.frontiersin.org June 2014 | Volume 8 | Article 209 | 5

Raboni et al. EMDR, sleep and PTSD patients

SLEEP PARAMETERSResults obtained in the polysomnography are shown in Figure 3and Table 3 (non-significant results). Although statistical differ-ences were not detected by ANOVA for transitions from REMsleep to awakening and for REM density, the comparison betweenPTSD and CTL groups, before the onset of treatment, revealed aneffect size of 0.65 and 1.05, respectively, indicating medium andhigh clinical relevance. These differences were no longer presentafter the treatment. Table 4 shows the results of effect size for allparameters.

SLEEP EFFICIENCY (FIGURE 3A)There was an interaction between group and time-point[F(1, 22) = 4.74; p = 0.04]. PTSD patients had greater sleep effi-ciency after EMDR than before the treatment (p < 0.03).

WAKING AFTER SLEEP ONSET (WASO, FIGURE 3B)An interaction between group and time-point was detected[F(1, 22) = 6.51; p < 0.02]. Post hoc analysis showed that beforethe treatment PTSD patients spent more time awake than controlsubjects (p < 0.01); after the treatment these patients showed areduction of this parameter (p < 0.003), being indistinguishablefrom controls.

Throughout the treatment, there were differences only inmaximum HR in PTSD patients [F(1, 4) = 4.13; p < 0.02], with

Table 1 | Demographic data of the participants, regarding sex, age,

and years of education.

Groups Sex Age (y) Education (y)

Women Men

CTL (N = 11) 8 3 29.0 ± 4.4 17.8 ± 1.3

PTSD (N = 13) 10 3 30.5 ± 5.2 15.5 ± 4.3

CTL, Control; PTSD, Post-traumatic stress disorder.

higher rate in the first session than in all others (p < 0.03;Figure 4).

DISCUSSIONThe present study tested the hypothesis that treatment of PTSDwould improve the general well-being and sleep quality of affectedsubjects. The results showed that, indeed, PTSD patients hada significant improvement in all psychological parameters eval-uated. Interestingly, before treatment PTSD patients self-ratedtheir sleep very poorly, but objective measurements showed that,in fact, the most remarkable sleep alteration was a longer WASOtime than control volunteers.

The therapy chosen to treat PTSD symptoms helps patients toprocess the information about the traumatic event leading to aresolution and improvement of the condition (Levin et al., 1999)and its efficacy is attested by several studies using civilian popula-tions with reports of improvement after a few sessions (Wilsonet al., 1995; Rothbaum, 1997; Scheck et al., 1998; Bisson andAndrew, 2007). In the present study, patients required an aver-age of 5 sessions to reprocess the traumatic memory. Regardingtheir psychological profile, there was a robust improvement indepression and anxiety scores, which were significantly higherbefore the onset of treatment and became comparable to CTLsubjects at the end of treatment. It has been reported that PTSDpatients present hyperactivity of the noradrenergic system dur-ing waking (Southwick et al., 1999) and sleep (Mellman et al.,1995b). Interestingly, our patients exhibited a reduction of max-imum heart rate after the first EMDR session, and it has beenshown in previous studies that EMDR causes a shift in thesympathetic/parasympathetic activity toward increased parasym-pathetic tonus, reflected by decreased heart rate, decreased skingalvanic resistance and increased fingertip temperature in PTSDpatients (Dunn et al., 1996; Sack, 2007; Elofsson et al., 2008).Importantly, reduction of the sympathetic tonus may also beinvolved in extinction of fear memory that is observed withEMDR therapy. PTSD patients exhibit increased amygdala acti-vation both at resting state (Rabinak et al., 2011) or after stimulus

Table 2 | Psychological, stress perception and quality of life of Control (CTL) and posttraumatic stress disorder (PTSD) patients, assessed by

specific questionnaires.

Psychological aspects Before treatment After treatment

CTL (N = 11) PTSD (N = 13) CTL (N = 11) TEPT (N = 13)

Impact event scale 15.4 ± 6.5 27.0 ± 5.9* 10.1 ± 8.1� 7.8 ± 6.8�

BDI—depression 4.2 ± 4.4 17.4 ± 6.8* 2.2 ± 2.4 4.0 ± 4.6�

STA!—state 33.4 ± 8.6 45.5 ± 9.1* 34.1 ± 9.2 34.7 ± 9.1�

STAI—trait 34.1 ± 6.9 54.1 ± 10.0* 30.0 ± 7.6 36.1 ± 8.6�

RESTQ—general stress 0.9 ± 0.8 3.1 ± 1.3* 0.6 ± 0.7 1.0 ± 0.7�

RESTQ—emotional stress 1.2 ± 0.8 3.5 ± 1.3* 1.0 ± 0.9 1.5 ± 0.5�

RESTQ—social stress 1.1 ± 1.2 3.0 ± 1.1* 0.8 ± 1.1 1.2 ± 1.0�

RESTQ—fatigue 2.0 ± 1.6 3.5 ± 1.4* 1.9 ± 1.5 1.4 ± 1.2�

RESTQ—general well-being 4.4 ± 0.6 2.5 ± 1.2* 4.8 ± 0.7 4.6 ± 0.9�

SF36—quality of life 87.0 ± 6.4 54.2 ± 14.4* 89.0 ± 9.7 85.7 ± 8.0�

Scale of social adjustment 1.52 ± 0.3 2.24 ± 0.5* 1.44 ± 0.3 1.83 ± 0.5�

Values are presented as mean ± SD. Number of subjects per group is shown in parenthesis.*Different from CTL group (Mann-Whitney U Test); �Different from before treatment (Wilkoxon Rank Test).

Frontiers in Behavioral Neuroscience www.frontiersin.org June 2014 | Volume 8 | Article 209 | 6

Raboni et al. EMDR, sleep and PTSD patients

FIGURE 2 | Scores obtained from the Recovery-Stress-Questionnaire—

RESTQ-48 (A) and the Pittsburgh Sleep Quality Index (B) of control

(CTL, N = 11) and post-traumatic stress disorder (PTSD) patients

(N = 13). Data were obtained before and after EMDR therapy. Values areexpressed as mean ± s.e.m. ∗Different from CTL group; �Different frombefore treatment.

provocation (El Khoury-Malhame et al., 2011) and animal datashow that increased noradrenergic activity is a major mediatorof consolidation of fear memories by the amygdala (Roozendaalet al., 2009; Debiec et al., 2011). Therefore, reduced sympa-thetic activation may, at least in part, explain the improvementsobserved after EMDR. Recent data obtained from 10 PTSDpatients submitted to EMDR while being recorded by electroen-cephalogram, showed that this therapy shifted the activation oflimbic emotion-related structures to cortical regions involvedwith cognitive and associative processes, leading to improvementof the cognitive and sensorial processing of the traumatic event(Pagani et al., 2012). Only a few imaging studies have been car-ried out to evaluate neuroanatomical changes induced by EMDR.These studies report increased hippocampal volume in patientstreated for eight [case-study (Letizia et al., 2007)] or 12 weeks [29PTSD patients (Bossini et al., 2012)] and activation of the ante-rior cingulate gyrus and the left frontal lobe upon recall of thetraumatic event [case-study, three EMDR sessions (Levin et al.,1999)]. Despite the small sample size, these results seem to bepromising, given the role that these brain areas play in memoryand emotion (Levin et al., 1999; Bush et al., 2000).

PTSD patients underestimate their sleep efficiency and over-estimate sleep latency, but polysomnographic studies do notconsistently show differences in sleep pattern between patients

FIGURE 3 | Sleep efficiency (A) and waking after sleep onset (B), in

min, of control (CTL, N = 11) and post-traumatic stress disorder

(PTSD) patients (N = 13). Data were obtained before and after EMDRtherapy. Values are expressed as mean ± s.e.m. ∗Different from CTL group;�Different from before treatment.

and healthy volunteers (Dagan et al., 1991; Hurwitz et al., 1998;Engdahl et al., 2000), suggesting that the patients’ perception ofsleep quality may be impaired. In our sample, a similar phe-nomenon was observed. Almost all sleep parameters were statis-tically indistinguishable between patients and controls; nonethe-less, the effect size revealed that, indeed, PTSD patients presentedmore sleep disturbances than healthy volunteers, such as greaterapnea/hypopnea index, more transitions from REM sleep to wak-ing and greater REM density, in agreement with various previousreports (Ross et al., 1989, 1994; Breslau et al., 2004). Summationof these events may have led to the significantly longer wakingtime after sleep onset in PTSD patients observed before treatment.Studies concerning the sleep pattern of PTSD patients consensu-ally report problems of sleep continuity (Mellman et al., 1995b;Yetkin et al., 2010; Capaldi et al., 2011) and EMDR was capable ofrestoring WASO to normal levels, as seen in healthy volunteers.Moreover, this therapy also increased sleep efficiency, resultingin a more consolidated sleep, although before the onset of treat-ment PTSD patients displayed similar values compared to controlsubjects. Interestingly, pre-clinical work has shown that certainforms of stress induce REM sleep rebound (Rampin et al., 1991;Palma et al., 2000; Sanford et al., 2010), a phenomenon thoughtto be important for recovery from the adverse situation. However,there are some features related to the stimulus and to the subject

Frontiers in Behavioral Neuroscience www.frontiersin.org June 2014 | Volume 8 | Article 209 | 7

Raboni et al. EMDR, sleep and PTSD patients

Table 3 | Sleep parameters recorded before and 1 day after the end of EMDR therapy applied to control (CTL) and posttraumatic stress disorder

(PTSD) patients.

Sleep parameters Before After

CTL (N = 11) PTSD (N = 13) CTL (N = 11) PTSD (N = 13)

Sleep latency (min) 10.3 ± 6.1 8.3 ± 4.3 13.5 ± 15.6 5.8 ± 7.1REM sleep latency (min) 83.2 ± 36.5 81.2 ± 28.9 84.5 ± 39.4 91.4 ± 31.5N1 (%) 2.7 ± 2.4 3.9 ± 4.3 1.9 ± 1.2 2.8 ± 1.7N2 (%) 57.8 ± 6 54.7 ± 4.5 55.8 ± 6.8 54.8 ± 6.4N3 (%) 21.0 ± 6.0 22.2 ± 6.3 22.2 ± 7.8 21.7 ± 8.1Micro-arousals (n) 71.2 ± 25.4 80.1 ± 29.2 75.5 ± 28.1 72.3 ± 29.1Total sleep time (min) 383.1 ± 24.3 375.8 ± 57.3 377.4 ± 66.3 379.5 ± 47.9PLM (n/h) 0.6 ± 2.2 0.6 ± 2.1 0.6 ± 2.0 0.7 ± 2.1AHI (n/h) 2.1 ± 1.7 4.8 ± 6.7 2.8 ± 2.1 4.2 ± 6.2Transitions REM-waking 3.0 ± 1.7 4.8 ± 3.5 2.9 ± 1.8 3.8 ± 2.7Transitions REM-N1 0.4 ± 0.7 0.4 ± 0.6 0.6 ± 1.0 0.6 ± 0.8Transitions REM-N2 2.5 ± 0.9 2.4 ± 1.6 3.4 ± 2.2 2.5 ± 1.4REM density a 34 ± 18 62 ± 33 29 ± 21 26 ± 17

Values are presented as mean ± SD. Number of subjects per group is shown in parenthesis.aREM density was determined in 9 control subjects and 13 PTSD patients.

Table 4 | Cohen D effect size was calculated for all sleep parameters.

Sleep Within-group Between-group Between-group

parameters comparisons comparison comparison

before EMDR after EMDR

CTL PTSD CTL × PTSD CTL × PTSD

Sleep latency (min) 0.59 0.42 0.38 0.63

N 1 (%) 0.42 0.34 0.34 0.61

N 2 (%) 0.31 0.02 0.58 0.15N 3 (%) 0.17 0.07 0.20 0.06Latency to REM (min) 0.03 0.34 0.06 0.19REM sleep (%) 0.10 0.37 0.34 0.08Micro-arousals (n) 0.19 0.24 0.33 0.11WASO (min) 0.18 1.29 1.13 0.23Total sleep time (min) 0.11 0.07 0.17 0.04Sleep efficiency (%) 0.02 1.13 0.74 0.50

PLM (n/h) 0.00 0.05 0.24 0.20AHI (n/h) 0.50 0.0 0.58 0.45Transitions REM-waking 0.11 0.32 0.65 0.39Transitions REM-N 1 0.23 0.28 0.00 0.00Transitions REM-N 2 0.54 0.07 0.08 0.49REM density a 0.26 1.37 1.05 0.16

Comparisons were made within each group (before x after EMDR) and between

groups in each time-point. Bold blue values represent moderate clinical relevance

(values between 0.5 and 0.8), whereas those in red represent great clinical rele-

vance (above 0.8).aREM density was determined in 9 control subjects and 13 PTSD patients.

WASO, waking after sleep onset, PLM, periodic limb movements; AHI: apnea-

hypopnea index.

(anxiety level) that interfere with the sleep outcome (Sucheckiet al., 2012). In our sample, PTSD patients had higher scores ofboth trait and state anxiety, and this could be a psychologicaldisadvantage in stressful or traumatic situations, as shown by

FIGURE 4 | Minimum and maximum heart rate (bpm) obtained in

post-traumatic stress disorder (PTSD) patients in each EMDR session.

Values are expressed as mean ± SD of 13 patients. #Different from allother sessions.

mice and rat strains that display more anxiety-like behavior andfail to exhibit the characteristic increase in REM sleep time after amild stressor (Meerlo et al., 2001; Sanford et al., 2003; Tang et al.,2005). Although the experimental protocol used in the presentstudy did not allow assessment of post-trauma sleep, Mellmanet al. (2002) showed that consolidated periods of REM sleepwithin a month of a traumatic event lowered the probability ofaccident victims to develop PTSD.

Studies designed to investigate the effects of PTSD treatmentson objective sleep parameters are scarce. These treatments usuallyare successful for PTSD, but residual insomnia is often a com-plaint (Zayfert and Deviva, 2004; Belleville et al., 2011). A recentstudy, carried out to treat residual insomnia in PTSD patients,

Frontiers in Behavioral Neuroscience www.frontiersin.org June 2014 | Volume 8 | Article 209 | 8

Raboni et al. EMDR, sleep and PTSD patients

compared the effects of a specific CBT protocol for insomniawith a waitlist non-treated group and showed improvementsof insomnia and depression symptoms in treated, compared tonon-treated patients, although both groups presented improve-ment of PTSD symptoms at the end of treatment period (Talbotet al., 2014). The present approach differed from Talbot’s, becausewe intended to assess the efficacy of a treatment for PTSD onsleep parameters. Thus, we compared PTSD patients to healthyvolunteers who were also submitted to the therapy for three rea-sons. First, we wanted to rule out the possibility of a placeboeffect, which could have occurred just by the comforting feel-ing that patients experience for being taken care of. Second, wealso wanted to make sure that possible sleep changes would notbe due to habituation to sleep recording setting. Previous reportsindicate that PTSD outpatients are more sensitive to sleeping inan unknown place (Woodward et al., 1996; Ross et al., 1999)(also known as first night effect), therefore, habituation to thesleep recording setting could have precluded the results. Third, wewanted to have reference values for the assessed parameters andnot only compare the patients before and after the treatment, e.g.,improvement of the symptoms might not mean return to con-trol, healthy levels. The fact that EMDR induced changes only inPTSD patients and that they did not differ from controls at post-treatment time, indicated that this was a successful approach totest the proposed hypothesis of this study.

In conclusion, PTSD patients presented high levels of depres-sion and anxiety before treatment, whereas, after the therapyall variables were indistinguishable from those of control sub-jects. Moreover, some sleep impairments were also improvedby EMDR. Therefore, treatment of PTSD ameliorated the gen-eral well-being of the patients, but it is not possible, withinthe experimental design of this study, to establish cause-effectrelationships.

LIMITATIONS OF THE STUDYVarious criteria were applied in order to gather a more homoge-nous sample of PTSD patients, such as restrictions to any previoustherapy, to a single traumatic event, to the type of trauma and tothe time span between the traumatic event and onset of EMDR toa maximum of 5 years. This strategy resulted in a small numberof participants, which was worsened by the significant amountof drop-outs. Despite this drawback, we believe that such rigoradded credibility to the results.

A second limitation of this study refers to the selection of onetype of trauma, which hindered generalization of the effects ofEMDR on the outcomes reported in the present study. Althoughthis therapeutic approach has been used in several populations,this is the first study, to the best of our knowledge, to assessits effects on sleep. Therefore, the possibility of type of trauma-related biased effect exists, although this seems to be unlikely.

ACKNOWLEDGMENTSThe authors would like to thank Psychologist Leila ReginaRaboni for helping with the psychological evaluation and toDr. Alexandro Borges Guerra, Psychiatrist, who performed thepsychiatric evaluation of all subjects. We are also in debt withDr. Robert J. Handa, from the Department of Basic Medical

Science, The University of Arizona College of Medicine, Phoenix,AZ, for critical reading of this manuscript. This work wassupported by Associação Fundo de Incentivo à Pesquisa andFundação de Amparo à Pesquisa do Estado de São Paulo(FAPESP/CEPID grant # 98/14303-3). Sergio Tufik and DeborahSuchecki are recipients of fellowships from Conselho Nacionalde Desenvolvimento Científico e Tecnológico (CNPq). Part ofthese data was presented as an extended abstract at the sympo-sium Psychobiology of Posttraumatic Stress Disorder – A Decadeof Progress sponsored by the New York Academy of Sciencein 2005.

REFERENCESAASM. (1999). Sleep-related breathing disorders in adults: recommendations for

syndrome definition and measurement techniques in clinical research. Thereport of an American academy of Sleep Medicine task force. Sleep 22, 667–689.

ABIPEME. (2003). “Classificação socioeconômica: critério ABIPEME” (AssociaçãoBrasileira de Institutos de Pesquisa e Mercado)).

ASDA. (2003). American sleep disorders association standards of pratice com-mitte. Pratice parameters for the indications for polysonography and relatedprocedures. Indications for polysomnography task force. Sleep Med Rev 20,406–422.

Beck, A. T., Ward, C. H., Mendelson, M., Mock, J., and Erbaugh, J. (1961). Aninventory for measuring depression. Arch. Gen. Psychiatry 4, 561–571. doi:10.1001/archpsyc.1961.01710120031004

Belleville, G., Guay, S., and Marchand, A. (2011). Persistence of sleep distur-bances following cognitive-behavior therapy for posttraumatic stress disorder.J. Psychosom. Res. 70, 318–327. doi: 10.1016/j.jpsychores.2010.09.022

Bisson, J., and Andrew, M. (2007). Psychological treatment of post-traumaticstress disorder (PTSD). Cochrane Database Syst. Rev. 3:CD003388. doi:10.1002/14651858.CD003388

Bisson, J. I., Ehlers, A., Matthews, R., Pilling, S., Richards, D., and Turner,S. (2007). Psychological treatments for chronic post-traumatic stress disor-der. Systematic review and meta-analysis. Br. J. Psychiatry 190, 97–104. doi:10.1192/bjp.bp.106.021402

Blechert, J., Michael, T., Grossman, P., Lajtman, M., and Wilhelm, F.H. (2007). Autonomic and respiratory characteristics of posttraumaticstress disorder and panic disorder. Psychosom. Med. 69, 935–943. doi:10.1097/PSY.0b013e31815a8f6b

Bossini, L., Casolaro, I., Santarnecchi, E., Caterini, C., Koukouna, D., Fernandez,I., et al. (2012). Evaluation study of clinical and neurobiological efficacy ofEMDR in patients suffering from post-traumatic stress disorder. Riv. Psichiatr.47, 12–15. doi: 10.1708/1071.11733

Breslau, N., Kessler, R. C., Chilcoat, H. D., Schultz, L. R., Davis, G. C., and Andreski,P. (1998). Trauma and posttraumatic stress disorder in the community: the1996 Detroit area survey of trauma. Arch. Gen. Psychiatry 55, 626–632. doi:10.1001/archpsyc.55.7.626

Breslau, N., Roth, T., Burduvali, E., Kapke, A., Schultz, L., and Roehrs, T. (2004).Sleep in lifetime posttraumatic stress disorder: a community-based polysomno-graphic study. Arch. Gen. Psychiatry 61, 508–516. doi: 10.1001/archpsyc.61.5.508

Bryant, R. A., Creamer, M., O’donnell, M., Silove, D., and McFarlane, A. C. (2010).Sleep disturbance immediately prior to trauma predicts subsequent psychiatricdisorder. Sleep 33, 69–74.

Bush, G., Luu, P., and Posner, M. I. (2000). Cognitive and emotional influencesin anterior cingulate cortex. Trends Cogn. Sci. 4, 215–222. doi: 10.1016/S1364-6613(00)01483-2

Buysse, D. J., Reynolds, C. F., Monk, T. H., Berman, S. R., and Kupfer, D. J. (1989).The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practiceand research. Psychiatry Res. 28, 193–213. doi: 10.1016/0165-1781(89)90047-4

Capaldi, V. F. 2nd., Guerrero, M. L., and Killgore, W. D. (2011). Sleep disruptionsamong returning combat veterans from Iraq and Afghanistan. Mil. Med. 176,879–888. doi: 10.7205/MILMED-D-10-00440

Cohen, H., Kotler, M., Matar, M. A., Kaplan, Z., Miodownik, H., and Cassuto,Y. (1997). Power spectral analysis of heart rate variability in posttraumaticstress disorder patients. Biol. Psychiatry 41, 627–629. doi: 10.1016/S0006-3223(96)00525-2

Frontiers in Behavioral Neuroscience www.frontiersin.org June 2014 | Volume 8 | Article 209 | 9

Raboni et al. EMDR, sleep and PTSD patients

Creamer, M., Burgess, P., and McFarlane, A. C. (2001). Post-traumatic stress dis-order: findings from the Australian National Survey of Mental Health andWell-being. Psychol. Med. 31, 1237–1247. doi: 10.1017/S0033291701004287

Dagan, Y., Lavie, P., and Bleich, A. (1991). Elevated awakening thresholds in sleepstage 3-4 in war-related post-traumatic stress disorder. Biol. Psychiatry 30,618–622. doi: 10.1016/0006-3223(91)90031-G

Debiec, J., Bush, D. E., and Ledoux, J. E. (2011). Noradrenergic enhancementof reconsolidation in the amygdala impairs extinction of conditioned fear inrats–a possible mechanism for the persistence of traumatic memories in PTSD.Depress. Anxiety 28, 186–193. doi: 10.1002/da.20803

Del Ben, C. M., Vilela, J. A., Crippa, J. A., Hallak, J. E., Labate, C. M., and Zuardi,A. W. (2001). Confiabilidade da Entrevista Clínica Estruturada para o DSM-IV– Versão Clínica traduzida para o português. [Reliability of the structured inter-view for the DSM-IV-clinical scale translated to Portuguese]. Revista Brasileirade Psiquiatria 23, 156–159. doi: 10.1590/S1516-44462001000300008

DSM-IV. (1994). Diagnostic and Statistical Manual of Mental Disorders.Washington, DC: American Psychiatric Association.

Dunn, T. M., Schwartz, M., Hatfield, R. W., and Wiegele, M. (1996). Measuringeffectiveness of eye movement desensitization and reprocessing (EMDR) innon-clinical anxiety: a multi-subject, yoked-control design. J. Behav. Ther. Exp.Psychiatry 27, 231–239. doi: 10.1016/S0005-7916(96)00034-1

El Khoury-Malhame, M., Reynaud, E., Soriano, A., Michael, K., Salgado-Pineda, P., Zendjidjian, X., et al. (2011). Amygdala activity correlateswith attentional bias in PTSD. Neuropsychologia 49, 1969–1973. doi:10.1016/j.neuropsychologia.2011.03.025

Elofsson, U. O., Von Schèele, B., Theorell, T., and Söndergaard, H. P. (2008).Physiological correlates of eye movement desensitization and reprocessing.J. Anxiety Disord. 22, 622–634. doi: 10.1016/j.janxdis.2007.05.012

Engdahl, B. E., Eberly, R. E., Hurwitz, T. D., Mahowald, M. W., and Blake, J.(2000). Sleep in a community sample of elderly war veterans with and withoutposttraumatic stress disorder. Biol. Psychiatry 47, 520–525. doi: 10.1016/S0006-3223(99)00201-2

Foa, E. B., and Meadows, E. A. (1997). Psychosocial treatments for posttrau-matic stress disorder: a critical review. Annu. Rev. Psychol. 48, 449–480. doi:10.1146/annurev.psych.48.1.449

Galovski, T. E., Monson, C., Bruce, S. E., and Resick, P. A. (2009). Does cognitive-behavioral therapy for PTSD improve perceived health and sleep impairment?J. Trauma. Stress 22, 197–204. doi: 10.1002/jts.20418

Germain, A., Richardson, R., Moul, D. E., Mammen, O., Haas, G., Forman, S.D., et al. (2012). Placebo-controlled comparison of prazosin and cognitive-behavioral treatments for sleep disturbances in US Military Veterans.J. Psychosom. Res. 72, 89–96. doi: 10.1016/j.jpsychores.2011.11.010

Hefez, A., Metz, L., and Lavie, P. (1987). Long-term effects of extreme situationalstress on sleep and dreaming. Am. J. Psychiatry 144, 344–347.

Horowitz, M., Wilner, N., and Alvares, W. (1979). Impact of Event Scale: a measureof subjective stress. Psychosom. Med. 41, 209–218. doi: 10.1097/00006842-197905000-00004

Hurwitz, T. D., Mahowald, M. W., Kuskowski, M., and Engdahl, B. E. (1998).Polysomnographic sleep is not clinically impaired in Vietnam combat veteranswith chronic posttraumatic stress disorder. Biol. Psychiatry 44, 1066–1073. doi:10.1016/S0006-3223(98)00089-4

Kato, H., Asukai, N., Miyake, Y., Minakawa, K., and Nishiyama, A. (1996). Post-traumatic symptoms among younger and elderly evacuees in the early stagesfollowing the 1995 Hanshin-Awaji earthquake in Japan. Acta Psychiatr. Scand.93, 477–481. doi: 10.1111/j.1600-0447.1996.tb10680.x

Kellmann, M., and Kallus, K. W. (2001). Recovery Stress Questionnaire for Athletes;User Manual. Champaign, IL: Human Kinetics.

Kessler, R. C., Sonnega, A., Bromet, E., Hughes, M., and Nelson, C. B. (1995).Posttraumatic stress disorder in the National Comorbidity Survey. Arch. Gen.Psychiatry 52, 1048–1060. doi: 10.1001/archpsyc.1995.03950240066012

Krakow, B., Hollifield, M., Johnston, L., Koss, M., Schrader, R., Warner, T. D., et al.(2001a). Imagery rehearsal therapy for chronic nightmares in sexual assault sur-vivors with posttraumatic stress disorder: a randomized controlled trial. JAMA286, 537–545. doi: 10.1001/jama.286.5.537

Krakow, B., Johnston, L., Melendrez, D., Hollifield, M., Warner, T. D., Chavez-Kennedy, D., et al. (2001b). An open-label trial of evidence-based cog-nitive behavior therapy for nightmares and insomnia in crime victimswith PTSD. Am. J. Psychiatry 158, 2043–2047. doi: 10.1176/appi.ajp.158.12.2043

Krakow, B. J., Melendrez, D. C., Johnston, L. G., Clark, J. O., Santana, E. M., Warner,T. D., et al. (2002). Sleep dynamic therapy for cerro grande fire evacuees withposttraumatic stress symptoms: a preliminary report. J. Clin. Psychiatry 63,673–684. doi: 10.4088/JCP.v63n0804

Letizia, B., Andrea, F., and Paolo, C. (2007). Neuroanatomical changes aftereye movement desensitization and reprocessing (EMDR) treatment in post-traumatic stress disorder. J. Neuropsychiatry Clin. Neurosci. 19, 475–476. doi:10.1176/appi.neuropsych.19.4.475

Levin, P., Lazrove, S., and Van Der Kolk, B. (1999). What psychological testing andneuroimaging tell us about the treatment of posttraumatic stress disorder by eyemovement desensitization and reprocessing. J. Anxiety Disord. 13, 159–172. doi:10.1016/S0887-6185(98)00045-0

Meerlo, P., Easton, A., Bergmann, B. M., and Turek, F. W. (2001). Restraint increasesprolactin and REM sleep in C57BL/6J mice but not in BALB/cJ mice. Am. J.Physiol. Regul. Integr. Comp. Physiol. 281, R846–R854.

Mellman, T. A., Bustamante, V., Fins, A. I., Pigeon, W. R., and Nolan, B. (2002).REM sleep and the early development of posttraumatic stress disorder. Am. J.Psychiatry 159, 1696–1701. doi: 10.1176/appi.ajp.159.10.1696

Mellman, T. A., David, D., Kulick-Bell, R., Hebding, J., and Nolan, B. (1995a).Sleep disturbance and its relationship to psychiatric morbidity after HurricaneAndrew. Am. J. Psychiatry 152, 1659–1663.

Mellman, T. A., Kulick-Bell, R., Ashlock, L. E., and Nolan, B. (1995b). Sleepevents among veterans with combat-related posttraumatic stress disorder. Am.J. Psychiatry 152, 110–115.

Mellman, T. A., Kumar, A., Kulick-Bell, R., Kumar, M., and Nolan, B. (1995c).Nocturnal/daytime urine noradrenergic measures and sleep in combat-relatedPTSD. Biol. Psychiatry 38, 174–179. doi: 10.1016/0006-3223(94)00238-X

Norris, F. H., Perilla, J. L., and Murphy, A. D. (2001). Postdisaster stress in theUnited States and Mexico: a cross-cultural test of the multicriterion conceptualmodel of posttraumatic stress disorder. J. Abnorm. Psychol. 110, 553–563. doi:10.1037/0021-843X.110.4.553

Ohayon, M. M., and Shapiro, C. M. (2000). Sleep disturbances and psychiatric dis-orders associated with posttraumatic stress disorder in the general population.Compr. Psychiatry 41, 469–478. doi: 10.1053/comp.2000.16568

Olff, M., Langeland, W., and Gersons, B. P. (2005). The psychobiology ofPTSD: coping with trauma. Psychoneuroendocrinology 30, 974–982. doi:10.1016/j.psyneuen.2005.04.009

Pagani, M., Di Lorenzo, G., Verardo, A. R., Nicolais, G., Monaco, L., Lauretti, G.,et al. (2012). Neurobiological correlates of EMDR monitoring - an EEG study.PLoS ONE 7:e45753. doi: 10.1371/journal.pone.0045753

Palma, B. D., Suchecki, D., and Tufik, S. (2000). Differential effects of acute coldand footshock on the sleep of rats. Brain Res. 861, 97–104. doi: 10.1016/S0006-8993(00)02024-2

Pillar, G., Malhotra, A., and Lavie, P. (2000). Post-traumatic stress dis-order and sleep-what a nightmare! Sleep Med. Rev. 4, 183–200. doi:10.1053/smrv.1999.0095

Rabinak, C. A., Angstadt, M., Welsh, R. C., Kenndy, A. E., Lyubkin, M., Martis,B., et al. (2011). Altered amygdala resting-state functional connectivity inpost-traumatic stress disorder. Front. Psychiatry 2:62. doi: 10.3389/fpsyt.2011.00062

Rampin, C., Cespuglio, R., Chastrette, N., and Jouvet, M. (1991). Immobilisationstress induces a paradoxical sleep rebound in rat. Neurosci. Lett. 126, 113–118.doi: 10.1016/0304-3940(91)90532-X

Rechtschaffen, A., and Kales, A. (1968). A Manual of Standardiled Terminology,Techniques and Scoring System for Sleep Stages of Human Subjects. Los Angeles,CA: UCLA Brain Information service/Brain Research Institute.

Rhudy, J. L., Davis, J. L., Williams, A. E., McCabe, K. M., Bartley, E. J., Byrd,P. M., et al. (2010). Cognitive-behavioral treatment for chronic nightmares intrauma-exposed persons: assessing physiological reactions to nightmare-relatedfear. J. Clin. Psychol. 66, 365–382. doi: 10.1002/jclp.20656

Roozendaal, B., McEwen, B. S., and Chattarji, S. (2009). Stress, memory and theamygdala. Nat. Rev. Neurosci. 10, 423–433. doi: 10.1038/nrn2651

Ross, R. J., Ball, W. A., Dinges, D. F., Kribbs, N. B., Morrison, A. R., Silver, S. M.,et al. (1994). Rapid eye movement sleep disturbance in posttraumatic stressdisorder. Biol. Psychiatry 35, 195–202. doi: 10.1016/0006-3223(94)91152-5

Ross, R. J., Ball, W. A., Sanford, L. D., Morrison, A. R., Dinges, D. F., Silver, S.M., et al. (1999). Rapid eye movement sleep changes during the adaptationnight in combat veterans with posttraumatic stress disorder. Biol. Psychiatry 45,938–941. doi: 10.1016/S0006-3223(98)00233-9

Frontiers in Behavioral Neuroscience www.frontiersin.org June 2014 | Volume 8 | Article 209 | 10

Raboni et al. EMDR, sleep and PTSD patients

Ross, R. J., Ball, W. A., Sullivan, K. A., and Caroff, S. N. (1989). Sleep disturbanceas the hallmark of posttraumatic stress disorder. Am. J. Psychiatry 146, 697–707.

Rothbaum, B. O. (1997). A controlled study of eye movement desensitization andreprocessing in the treatment of posttraumatic stress disordered sexual assaultvictims. Bull. Menninger Clin. 61, 317–334.

Rothbaum, B. O., Kozak, M. J., Foa, E. B., and Whitaker, D. J. (2001). Posttraumaticstress disorder in rape victims: autonomic habituation to auditory stimuli.J. Trauma. Stress 14, 283–293. doi: 10.1023/A:1011160800958

Sack, M. (2007). Assessment of psychophysiological stress reactions during a trau-matic reminder in patients treated with EMDR. J. EMDR Practice Res. 1, 15–23.doi: 10.1891/1933-3196.1.1.15

Sanford, L. D., Yang, L., and Tang, X. (2003). Influence of contextual fear on sleepin mice: a strain comparison. Sleep 26, 527–540.

Sanford, L. D., Yang, L., Wellman, L. L., Liu, X., and Tang, X. (2010). Differentialeffects of controllable and uncontrollable footshock stress on sleep in mice. Sleep33, 621–630.

Scheck, M. M., Schaeffer, J. A., and Gillette, C. (1998). Brief psychologicalintervention with traumatized young women: the efficacy of eye move-ment desensitization and reprocessing. J. Trauma. Stress 11, 25–44. doi:10.1023/A:1024400931106

Shapiro, F. (1995). Eye Movement Desensitization and Reprocessing: Basic Principles,Protocols and Procedures. New York, NY: Guilford.

Shapiro, F. (1996). Eye movement desensitization and reprocessing (EMDR): eval-uation of controlled PTSD research. J. Behav. Ther. Exp. Psychiatry 27, 209–218.doi: 10.1016/S0005-7916(96)00029-8

Shapiro, F. (1999). Eye Movement Desensitization and Reprocessing (EMDR)and the anxiety disorders: clinical and research implications of an integratedpsychotherapy treatment. J. Anxiety Disord. 13, 35–67. doi: 10.1016/S0887-6185(98)00038-3

Southwick, S. M., Bremner, J. D., Rasmusson, A., Morgan, C. A., 3rd, Arnsten, A.,and Charney, D. S. (1999). Role of norepinephrine in the pathophysiology andtreatment of posttraumatic stress disorder. Biol. Psychiatry 46, 1192–1204. doi:10.1016/S0006-3223(99)00219-X

Spielberger, C. D., Gorsuch, R. L., and Lushene, R. E. (1970). Manual for the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press.

Spoormaker, V. I., and Montgomery, P. (2008). Disturbed sleep in post-traumaticstress disorder: secondary symptom or core feature? Sleep Med. Rev. 12,169–184. doi: 10.1016/j.smrv.2007.08.008

Stein, M. B., Walker, J. R., Hazen, A. L., and Forde, D. R. (1997). Full and par-tial posttraumatic stress disorder: findings from a community survey. Am. J.Psychiatry 154, 1114–1119.

Suchecki, D., Tiba, P. A., and Machado, R. B. (2012). REM sleep reboundas an adaptive response to stressful situations. Front. Neurol. 3:41. doi:10.3389/fneur.2012.00041

Talbot, L. S., Maguen, S., Metzler, T. J., Schmitz, M., McCaslin, S. E., Richards,A., et al. (2014). Cognitive behavioral therapy for insomnia in posttrau-matic stress disorder: a randomized controlled trial. Sleep 37, 327–341. doi:10.5665/sleep.3408

Tang, X., Yang, L., and Sanford, L. D. (2005). Rat strain differences in freezing andsleep alterations associated with contextual fear. Sleep 28, 1235–1244.

Van Etten, M., and Taylor, S. (1998). Comparative efficacy of treatments for post-traumatic stress disorder: a meta-analysis. Clin. Psychol. Psychother. 5, 126–144.

Van Liempt, S. (2012). Sleep disturbances and PTSD: a perpetual circle? Eur. J.Psychotraumatol. 3, 1–9. doi: 10.3402/ejpt.v3i0.19142

Ware, J. E., and Sherbourne, C. D. (1992). The MOS 36 items short-form healthsurvery (SF-36) - 1. Conceptual framework and item selection. Med. Care 30,473–483. doi: 10.1097/00005650-199206000-00002

Weissman, M. M., and Bothwell, S. (1976). Assessment of social adjustmentby patient self-report. Arch. Gen. Psychiatry 33:1111–1115 doi: 10.1001/arch-psyc.1976.01770090101010

Wilson, S. A., Becker, L. A., and Tinker, R. H. (1995). Eye movement desensitizationand reprocessing (EMDR) treatment for psychologically traumatized individu-als. J. Consult. Clin. Psychol. 63, 928–937. doi: 10.1037/0022-006X.63.6.928

Woodward, S. H., Bliwise, D. L., Friedman, M. J., and Gusman, F. D. (1996). Firstnight effects in post-traumatic stress disorder inpatients. Sleep 19, 312–317.

Yetkin, S., Aydin, H. and Ozgen, F. (2010). Polysomnography in patients withpost-traumatic stress disorder. Psychiatry Clin. Neurosci. 64, 309–317. doi:10.1111/j.1440-1819.2010.02084.x

Zayfert, C., and Deviva, J. C. (2004). Residual insomnia following cogni-tive behavioral therapy for PTSD. J. Trauma. Stress 17, 69–73. doi:10.1023/B:JOTS.0000014679.31799.e7

Conflict of Interest Statement: The authors declare that the research was con-ducted in the absence of any commercial or financial relationships that could beconstrued as a potential conflict of interest.

Received: 03 April 2014; accepted: 22 May 2014; published online: 10 June 2014.Citation: Raboni MR, Alonso FFD, Tufik S and Suchecki D (2014) Improvement ofmood and sleep alterations in posttraumatic stress disorder patients by eye movementdesensitization and reprocessing. Front. Behav. Neurosci. 8:209. doi: 10.3389/fnbeh.2014.00209This article was submitted to the journal Frontiers in Behavioral Neuroscience.Copyright © 2014 Raboni, Alonso, Tufik and Suchecki. This is an open-access articledistributed under the terms of the Creative Commons Attribution License (CC BY).The use, distribution or reproduction in other forums is permitted, provided theoriginal author(s) or licensor are credited and that the original publication in thisjournal is cited, in accordance with accepted academic practice. No use, distribution orreproduction is permitted which does not comply with these terms.

Frontiers in Behavioral Neuroscience www.frontiersin.org June 2014 | Volume 8 | Article 209 | 11